Broadly Tuned Response Properties of Diverse Inhibitory Neuron Subtypes in Mouse Visual Cortex

Neuron

Volumn 67, Issue 5, 2010, Pages 858-871

  Kerlin, Aaron M ^a   Andermann, Mark L ^a   Berezovskii, Vladimir K ^a   Reid, R Clay ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; 4 AMINOBUTYRIC ACID; CALCIUM; EGTAZIC ACID; FLUORESCENT DYE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; EX VIVO STUDY; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MOUSE; NERVE CELL; NEUROIMAGING; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VISUAL CORTEX; VISUAL STIMULATION; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CLASSIFICATION; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL INHIBITION; ORIENTATION; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; THREE DIMENSIONAL IMAGING; TRANSGENIC MOUSE; VISUAL SYSTEM;

ANIMALS; CALCIUM; EGTAZIC ACID; FLUORESCENT DYES; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; IMAGING, THREE-DIMENSIONAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; ORIENTATION; PARVALBUMINS; PHOTIC STIMULATION; SOMATOSTATIN; VASOACTIVE INTESTINAL PEPTIDE; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 77956336542     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.08.002     Document Type: Article

References (92)

1. Ahmed B., Anderson J.C., Martin K.A.C., Nelson J.C. Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J. Comp. Neurol. 1997, 380:230-242.
2. Andermann M.L., Moore C.I. A somatotopic map of vibrissa motion direction within a barrel column. Nat. Neurosci. 2006, 9:543-551.
3. Andermann M.L., Kerlin A.M., Reid R.C. Chronic cellular imaging of mouse visual cortex during operant behavior and passive viewing. Frontiers in Cellular Neuroscience 2010, 4:3.
4. Ascoli G.A., Alonso-Nanclares L., Anderson S.A., Barrionuevo G., Benavides-Piccione R., Burkhalter A., Buzsáki G., Cauli B., Defelipe J., Fairén A., et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 2008, 9:557-568. Petilla Interneuron Nomenclature Group.
5. Azouz R., Gray C.M., Nowak L.G., McCormick D.A. Physiological properties of inhibitory interneurons in cat striate cortex. Cereb. Cortex 1997, 7:534-545.
6. Bandyopadhyay S., Shamma S.A., Kanold P.O. Dichotomy of functional organization in the mouse auditory cortex. Nat. Neurosci. 2010, 13:361-368.
7. Beierlein M., Gibson J.R., Connors B.W. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 2000, 3:904-910.
8. Bonhoeffer T., Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 1991, 353:429-431.
9. Bousfield J.D. Columnar organisation and the visual cortex of the rabbit. Brain Res. 1977, 136:154-158.
10. Burkhalter A. Many specialists for suppressing cortical excitation. Front Neurosci. 2008, 2:155-167.
11. Carandini M., Ferster D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 2000, 20:470-484.
12. Carandini M., Heeger D.J., Movshon J.A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 1997, 17:8621-8644.
13. Cardin J.A., Palmer L.A., Contreras D. Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex. J. Neurosci. 2007, 27:10333-10344.
14. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
15. Celio M.R., Heizmann C.W. Calcium-binding protein parvalbumin as a neuronal marker. Nature 1981, 293:300-302.
16. Cho K.H., Jang J.H., Jang H.J., Kim M.J., Yoon S.H., Fukuda T., Tennigkeit F., Singer W., Rhie D.J. Subtype-specific dendritic Ca2+ dynamics of inhibitory interneurons in the rat visual cortex. J. Neurophysiol. 2010, in press. Published online June 16, 2010. 10.1152/jn.00146.20100022-3077/10.
17. Connor J.R., Peters A. Vasoactive intestinal polypeptide-immunoreactive neurons in rat visual cortex. Neuroscience 1984, 12:1027-1044.
18. Dräger U.C. Receptive fields of single cells and topography in mouse visual cortex. J. Comp. Neurol. 1975, 160:269-290.
19. Fagiolini M., Fritschy J.M., Löw K., Möhler H., Rudolph U., Hensch T.K. Specific GABAA circuits for visual cortical plasticity. Science 2004, 303:1681-1683.
20. Fanselow E.E., Richardson K.A., Connors B.W. Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J. Neurophysiol. 2008, 100:2640-2652.
21. Feldman M.L., Peters A. The forms of non-pyramidal neurons in the visual cortex of the rat. J. Comp. Neurol. 1978, 179:761-793.
22. Férézou I., Cauli B., Hill E.L., Rossier J., Hamel E., Lambolez B. 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J. Neurosci. 2002, 22:7389-7397.
23. Garaschuk O., Milos R.I., Konnerth A. Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat. Protoc. 2006, 1:380-386.
24. Gentet L.J., Avermann M., Matyas F., Staiger J.F., Petersen C.C. Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 2010, 65:422-435.
25. Girman S.V., Sauvé Y., Lund R.D. Receptive field properties of single neurons in rat primary visual cortex. J. Neurophysiol. 1999, 82:301-311.
26. Goldberg J.H., Tamas G., Yuste R. Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation. J. Physiol. 2003, 551:49-65.
27. Grewe B.F., Langer D., Kasper H., Kampa B.M., Helmchen F. High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat. Methods 2010, 7:399-405.
28. Hawken M.J., Parker A.J. Spatial properties of neurons in the monkey striate cortex. Proc. R Soc. Lond. B Biol. Sci. 1987, 231:251-288.
29. Hestrin S., Galarreta M. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci. 2005, 28:304-309.
30. Hippenmeyer S., Vrieseling E., Sigrist M., Portmann T., Laengle C., Ladle D.R., Arber S. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 2005, 3:e159.
31. Hirsch J.A., Martinez L.M., Pillai C., Alonso J.M., Wang Q., Sommer F.T. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat. Neurosci. 2003, 6:1300-1308.
32. Histed M.H., Bonin V., Reid R.C. Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 2009, 63:508-522.
33. Holmgren C., Harkany T., Svennenfors B., Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. 2003, 551:139-153.
34. Jia H., Rochefort N.L., Chen X., Konnerth A. Dendritic organization of sensory input to cortical neurons in vivo. Nature 2010, 464:1307-1312.
35. Kameyama K., Sohya K., Ebina T., Fukuda A., Yanagawa Y., Tsumoto T. Difference in binocularity and ocular dominance plasticity between GABAergic and excitatory cortical neurons. J. Neurosci. 2010, 30:1551-1559.
36. Kara P., Boyd J.D. A micro-architecture for binocular disparity and ocular dominance in visual cortex. Nature 2009, 458:627-631.
37. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 1997, 7:476-486.
38. Kawaguchi Y., Shindou T. Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. J. Neurosci. 1998, 18:6963-6976.
39. Kerr J.N.D., Greenberg D., Helmchen F. Imaging input and output of neocortical networks in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:14063-14068.
40. Knott G.W., Holtmaat A., Trachtenberg J.T., Svoboda K., Welker E. A protocol for preparing GFP-labeled neurons previously imaged in vivo and in slice preparations for light and electron microscopic analysis. Nat. Protoc. 2009, 4:1145-1156.
41. Lauritzen T.Z., Miller K.D. Different roles for simple-cell and complex-cell inhibition in V1. J. Neurosci. 2003, 23:10201-10213.
42. Liu B.H., Li P., Li Y.T., Sun Y.J., Yanagawa Y., Obata K., Zhang L.I., Tao H.W. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J. Neurosci. 2009, 29:10520-10532.
43. Liu B.H., Li P., Sun Y.J., Li Y.T., Zhang L.I., Tao H.W. Intervening inhibition underlies simple-cell receptive field structure in visual cortex. Nat. Neurosci. 2010, 13:89-96.
44. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
45. Mangini N.J., Pearlman A.L. Laminar distribution of receptive field properties in the primary visual cortex of the mouse. J. Comp. Neurol. 1980, 193:203-222.
46. Mariño J., Schummers J., Lyon D.C., Schwabe L., Beck O., Wiesing P., Obermayer K., Sur M. Invariant computations in local cortical networks with balanced excitation and inhibition. Nat. Neurosci. 2005, 8:194-201.
47. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
48. Martin K.A.C., Somogyi P., Whitteridge D. Physiological and morphological properties of identified basket cells in the cat's visual cortex. Exp. Brain Res. 1983, 50:193-200.
49. McCormick D.A., Connors B.W., Lighthall J.W., Prince D.A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 1985, 54:782-806.
50. Mrsic-Flögel T.D., Hofer S.B., Ohki K., Reid R.C., Bonhoeffer T., Hübener M. Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. Neuron 2007, 54:961-972.
51. Nauhaus I., Benucci A., Carandini M., Ringach D.L. Neuronal selectivity and local map structure in visual cortex. Neuron 2008, 57:673-679.
52. Niell C.M., Stryker M.P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 2008, 28:7520-7536.
53. Niell C.M., Stryker M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 2010, 65:472-479.
54. Nimmerjahn A., Kirchhoff F., Kerr J.N., Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 2004, 1:31-37.
55. Nowak L.G., Sanchez-Vives M.V., McCormick D.A. Lack of orientation and direction selectivity in a subgroup of fast-spiking inhibitory interneurons: cellular and synaptic mechanisms and comparison with other electrophysiological cell types. Cereb. Cortex 2008, 18:1058-1078.
56. Ohki K., Chung S., Ch'ng Y.H., Kara P., Reid R.C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 2005, 433:597-603.
57. Ohki K., Chung S., Kara P., Hübener M., Bonhoeffer T., Reid R.C. Highly ordered arrangement of single neurons in orientation pinwheels. Nature 2006, 442:925-928.
58. Oliva A.A., Jiang M., Lam T., Smith K.L., Swann J.W. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 2000, 20:3354-3368.
59. Payne B.R., Berman N. Functional organization of neurons in cat striate cortex: variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. J. Neurophysiol. 1983, 49:1051-1072.
60. Peters A., Kara D.A. The neuronal composition of area 17 of rat visual cortex. II. The nonpyramidal cells. J. Comp. Neurol. 1985, 234:242-263.
61. Pologruto T.A., Sabatini B.L., Svoboda K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2003, 2:13.
62. Poo C., Isaacson J.S. Odor representations in olfactory cortex: " sparse" coding, global inhibition, and oscillations. Neuron 2009, 62:850-861.
63. Porter J.T., Cauli B., Tsuzuki K., Lambolez B., Rossier J., Audinat E. Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J. Neurosci. 1999, 19:5228-5235.
64. Reynolds J.H., Heeger D.J. The normalization model of attention. Neuron 2009, 61:168-185.
65. Ringach D.L., Shapley R.M., Hawken M.J. Orientation selectivity in macaque V1: diversity and laminar dependence. J. Neurosci. 2002, 22:5639-5651.
66. Rothschild G., Nelken I., Mizrahi A. Functional organization and population dynamics in the mouse primary auditory cortex. Nat. Neurosci. 2010, 13:353-360.
67. Sagdullaev B.T., DeMarco P.J., McCall M.A. Improved contact lens electrode for corneal ERG recordings in mice. Doc. Ophthalmol. 2004, 108:181-184.
68. Sakata S., Harris K.D. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 2009, 64:404-418.
69. Sawinski J., Wallace D.J., Greenberg D.S., Grossmann S., Denk W., Kerr J.N. Visually evoked activity in cortical cells imaged in freely moving animals. Proc. Natl. Acad. Sci. USA 2009, 106:19557-19562.
70. Schummers J., Mariño J., Sur M. Synaptic integration by V1 neurons depends on location within the orientation map. Neuron 2002, 36:969-978.
71. Simons D.J. Response properties of vibrissa units in rat SI somatosensory neocortex. J. Neurophysiol. 1978, 41:798-820.
72. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
73. Sohya K., Kameyama K., Yanagawa Y., Obata K., Tsumoto T. GABAergic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2+ imaging in transgenic mice. J. Neurosci. 2007, 27:2145-2149.
74. Somogyi P., Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 2005, 562:9-26.
75. Stettler D.D., Axel R. Representations of odor in the piriform cortex. Neuron 2009, 63:854-864.
76. Stosiek C., Garaschuk O., Holthoff K., Konnerth A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 2003, 100:7319-7324.
77. Swadlow H.A. Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties. J. Neurophysiol. 1988, 59:1162-1187.
78. Swindale N.V., Matsubara J.A., Cynader M.S. Surface organization of orientation and direction selectivity in cat area 18. J. Neurosci. 1987, 7:1414-1427.
79. Tamamaki N., Yanagawa Y., Tomioka R., Miyazaki J., Obata K., Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 2003, 467:60-79.
80. Usrey W.M., Sceniak M.P., Chapman B. Receptive fields and response properties of neurons in layer 4 of ferret visual cortex. J. Neurophysiol. 2003, 89:1003-1015.
81. Van Hooser S.D., Heimel J.A., Chung S., Nelson S.B., Toth L.J. Orientation selectivity without orientation maps in visual cortex of a highly visual mammal. J. Neurosci. 2005, 25:19-28.
82. Wahle P. Differential regulation of substance P and somatostatin in Martinotti cells of the developing cat visual cortex. J. Comp. Neurol. 1993, 329:519-538.
83. Wörgötter F., Eysel U.T. Quantitative determination of orientational and directional components in the response of visual cortical cells to moving stimuli. Biol. Cybern. 1987, 57:349-355.
84. Xiang Z., Huguenard J.R., Prince D.A. Cholinergic switching within neocortical inhibitory networks. Science 1998, 281:985-988.
85. Xu X., Callaway E.M. Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J. Neurosci. 2009, 29:70-85.
86. Xu X., Roby K.D., Callaway E.M. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J. Comp. Neurol. 2006, 499:144-160.
87. Xu X., Roby K.D., Callaway E.M. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 2009, 518:389-404.
88. Yaksi E., Friedrich R.W. Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nat. Methods 2006, 3:377-383.
89. Yoshimura Y., Callaway E.M. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat. Neurosci. 2005, 8:1552-1559.
90. Zhu Y., Zhu J.J. Rapid arrival and integration of ascending sensory information in layer 1 nonpyramidal neurons and tuft dendrites of layer 5 pyramidal neurons of the neocortex. J. Neurosci. 2004, 24:1272-1279.
91. Zhu Y., Stornetta R.L., Zhu J.J. Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons. J. Neurosci. 2004, 24:5101-5108.
92. Zipfel W.R., Williams R.M., Webb W.W. Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 2003, 21:1369-1377.